Transferrin adsorption onto PLGA nanoparticles governs their interaction with biological systems from blood circulation to brain cancer cells

Pharmaceutical Research

Volumn 29, Issue 6, 2012, Pages 1495-1505

  Chang, Jiang ^a,b   Paillard, Archibald ^c,d   Passirani, Catherine ^c,d   Morille, Marie ^c,d   Benoit, Jean Pierre ^c,d   Betbeder, Didier ^a,b   Garcion, Emmanuel ^c,d,e  

^a IMPECS IMPact de l Environnement Chimique sur la Santé humaine   (France)

^b UNIVERSITÉ D'ARTOIS   (France)

^c UNIVERSITÉ D'ANGERS   (France)

^d INSERM   (France)

^e ANGERS UNIVERSITY HOSPITAL   (France)

Author keywords

blood brain barrier; central nervous system; glioma; PLGA nanocarriers; stealth; targeting

Indexed keywords

NANOPARTICLE; POLYGLACTIN; TRANSFERRIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOCOMPATIBILITY; BLOOD BRAIN BARRIER; BRAIN CANCER; CANCER CELL; CAVEOLA; CELL DIFFERENTIATION; CONTROLLED STUDY; DRUG DELIVERY SYSTEM; ENDOCYTOSIS; ENDOTHELIUM CELL; HALF LIFE TIME; HUMAN; HUMAN CELL; HYDRODYNAMICS; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; MACROPHAGE; MATERIAL COATING; MONOCYTE; MORPHOMETRICS; MOUSE; NANOMEDICINE; NONHUMAN; PARTICLE SIZE; POROSITY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RAT; SURFACE PROPERTY; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL;

ADSORPTION; ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN NEOPLASMS; CAPILLARY PERMEABILITY; CAVEOLAE; CELL LINE, TUMOR; CHEMISTRY, PHARMACEUTICAL; CLATHRIN; DRUG CARRIERS; DRUG COMPOUNDING; ENDOCYTOSIS; FEMALE; GLIOMA; HALF-LIFE; INJECTIONS, INTRAVENOUS; LACTIC ACID; MACROPHAGES; MICE; MONOCYTES; NANOPARTICLES; NANOTECHNOLOGY; POLYGLYCOLIC ACID; RATS; RATS, INBRED F344; RECEPTORS, TRANSFERRIN; TECHNOLOGY, PHARMACEUTICAL; TISSUE DISTRIBUTION; TRANSFERRIN;

EID: 84862638523     PISSN: 07248741     EISSN: 1573904X     Source Type: Journal    
DOI: 10.1007/s11095-011-0624-1     Document Type: Article

References (71)

1. R Stupp WP Mason MJ van den Bent M Weller B Fisher MJ Taphoorn, et al. 2005 Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma N Engl J Med 352 10 987 96 15758009 10.1056/NEJMoa043330 1:CAS:528: DC%2BD2MXit1Wksbk%3D
2. D Peer JM Karp S Hong OC Farokhzad R Margalit R Langer 2007 Nanocarriers as an emerging platform for cancer therapy Nat Nanotechnol 2 12 751 60 18654426 10.1038/nnano.2007.387 1:CAS:528:DC%2BD2sXhtlyktL%2FI
3. RA Sells RR Owen RR New IT Gilmore 1987 Reduction in toxicity of doxorubicin by liposomal entrapment Lancet 2 8559 624 5 2887906 10.1016/S0140-6736(87)93011-X 1:STN:280:DyaL2szhsVSnug%3D%3D
4. A Rahman J Treat JK Roh LA Potkul WG Alvord D Forst, et al. 1990 A phase I clinical trial and pharmacokinetic evaluation of liposome-encapsulated doxorubicin J Clin Oncol 8 6 1093 100 2348224 1:STN:280:DyaK3c3ntV2juw%3D%3D
5. JW Cowens PJ Creaven WR Greco DE Brenner Y Tung M Ostro, et al. 1993 Initial clinical (phase I) trial of TLC D-99 (doxorubicin encapsulated in liposomes) Cancer Res 53 12 2796 802 8504422 1:STN:280:DyaK3s3nvVKkuw%3D%3D
6. A Gabizon R Catane B Uziely B Kaufman T Safra R Cohen, et al. 1994 Prolonged circulation time and enhanced accumulation in malignant exudates of doxorubicin encapsulated in polyethylene-glycol coated liposomes Cancer Res 54 4 987 92 8313389 1:CAS:528:DyaK2cXhslegs70%3D
7. G Storm MT ten Kate PK Working IA Bakker-Woudenberg 1998 Doxorubicin entrapped in sterically stabilized liposomes: effects on bacterial blood clearance capacity of the mononuclear phagocyte system Clin Cancer Res 4 1 111 5 9516959 1:CAS:528:DyaK1cXmtFSmuw%3D%3D
8. R Gref Y Minamitake MT Peracchia V Trubetskoy V Torchilin R Langer 1994 Biodegradable long-circulating polymeric nanospheres Science 263 5153 1600 3 8128245 10.1126/science.8128245 1:CAS:528:DyaK2cXit1KktLc%3D
9. P Couvreur G Barratt E Fattal P Legrand C Vauthier 2002 Nanocapsule technology: a review Crit Rev Ther Drug Carrier Syst 19 2 99 134 12197610 10.1615/CritRevTherDrugCarrierSyst.v19.i2.10 1:CAS:528:DC%2BD38XntFSksbg%3D
10. RH Muller CM Keck 2004 Challenges and solutions for the delivery of biotech drugs-a review of drug nanocrystal technology and lipid nanoparticles J Biotechnol 113 1-3 151 70 15380654 10.1016/j.jbiotec.2004.06.007 1:CAS:528:DC%2BD2cXnslOhtL4%3D
11. E Garcion A Lamprecht B Heurtault A Paillard A Aubert-Pouessel B Denizot, et al. 2006 A new generation of anticancer, drug-loaded, colloidal vectors reverses multidrug resistance in glioma and reduces tumor progression in rats Mol Cancer Ther 5 7 1710 22 16891457 10.1158/1535-7163.MCT-06-0289 1:CAS:528:DC%2BD28XnslWksLo%3D
12. F Lacoeuille E Garcion JP Benoit A Lamprecht 2007 Lipid nanocapsules for intracellular drug delivery of anticancer drugs J Nanosci Nanotechno 7 12 4612 7 1:CAS:528:DC%2BD1cXhtFegu70%3D
13. M Pereira de Oliveira E Garcion N Venisse JP Benoit W Couet JC Olivier 2005 Tissue distribution of indinavir administered as solid lipid nanocapsule formulation in mdr1a (+/+) and mdr1a (-/-) CF-1 mice Pharm Res 22 11 1898 905 16132350 10.1007/s11095-005-7147-6 1:CAS:528:DC%2BD2MXhtFChs7nI
14. E Allard F Hindre C Passirani L Lemaire N Lepareur N Noiret, et al. 2008 188Re-loaded lipid nanocapsules as a promising radiopharmaceutical carrier for internal radiotherapy of malignant gliomas Eur J Nucl Med Mol Imaging 35 10 1838 46 18465130 10.1007/s00259-008-0735-z 1:CAS:528:DC%2BD1cXhtFCjtb3N
15. E Allard C Passirani E Garcion P Pigeon A Vessieres G Jaouen, et al. 2008 Lipid nanocapsules loaded with an organometallic tamoxifen derivative as a novel drug-carrier system for experimental malignant gliomas J Control Release 130 2 146 53 18582507 10.1016/j.jconrel.2008.05.027 1:CAS:528:DC%2BD1cXhtVais7rO
16. NY Rapoport AM Kennedy JE Shea CL Scaife KH Nam 2009 Controlled and targeted tumor chemotherapy by ultrasound-activated nanoemulsions/microbubbles J Control Release 138 3 268 76 19477208 10.1016/j.jconrel.2009.05.026 1:CAS:528:DC%2BD1MXpvFCmtro%3D
17. A Paillard C Passirani P Saulnier M Kroubi E Garcion JP Benoit, et al. 2010 Positively-charged, porous, polysaccharide nanoparticles loaded with anionic molecules behave as 'stealth' cationic nanocarriers Pharm Res 27 1 126 33 19851846 10.1007/s11095-009-9986-z 1:CAS:528:DC%2BD1MXhtlShsr3O
18. E Roger F Lagarce E Garcion JP Benoit 2009 Lipid nanocarriers improve paclitaxel transport throughout human intestinal epithelial cells by using vesicle-mediated transcytosis J Control Release 140 2 174 81 19699246 10.1016/j.jconrel.2009.08.010 1:CAS:528:DC%2BD1MXhtlOks73I
19. E Roger F Lagarce E Garcion JP Benoit 2010 Reciprocal competition between lipid nanocapsules and P-gp for paclitaxel transport across Caco-2 cells Eur J Pharm Sci 40 5 422 9 20438839 10.1016/j.ejps.2010.04.015 1:CAS:528: DC%2BC3cXnvVOrsbc%3D
20. C Lemarchand R Gref C Passirani E Garcion B Petri R Muller, et al. 2006 Influence of polysaccharide coating on the interactions of nanoparticles with biological systems Biomaterials 27 1 108 18 16118015 10.1016/j.biomaterials. 2005.04.041 1:CAS:528:DC%2BD2MXpsF2jsLY%3D
21. A Beduneau P Saulnier N Anton F Hindre C Passirani H Rajerison, et al. 2006 Pegylated nanocapsules produced by an organic solvent-free method: Evaluation of their stealth properties Pharm Res 23 9 2190 9 16952009 10.1007/s11095-006-9061-y 1:CAS:528:DC%2BD28XptVaisb0%3D
22. S Vinchon-Petit D Jarnet A Paillard JP Benoit E Garcion P Menei 2010 In vivo evaluation of intracellular drug-nanocarriers infused into intracranial tumours by convection-enhanced delivery: distribution and radiosensitisation efficacy J Neurooncol 97 2 195 205 19768659 10.1007/s11060-009-0012-4 1:CAS:528:DC%2BC3cXjtFygsLo%3D
23. A Paillard F Hindre C Vignes-Colombeix JP Benoit E Garcion 2010 The importance of endo-lysosomal escape with lipid nanocapsules for drug subcellular bioavailability Biomaterials 31 29 7542 54 20630585 10.1016/j.biomaterials. 2010.06.024 1:CAS:528:DC%2BC3cXpsV2qtL0%3D
24. Weyland M, Manero F, Paillard A, Gree D, Viault G, Jarnet D, et al. Mitochondrial targeting by use of lipid nanocapsules loaded with SV30, an analogue of the small-molecule Bcl-2 inhibitor HA14-1. J Control Release 2011.
25. AH Faraji P Wipf 2009 Nanoparticles in cellular drug delivery Bioorg Med Chem 17 8 2950 62 19299149 10.1016/j.bmc.2009.02.043 1:CAS:528: DC%2BD1MXksVWlur0%3D
26. SM Moghimi AC Hunter JC Murray 2005 Nanomedicine: current status and future prospects FASEB J 19 3 311 30 15746175 10.1096/fj.04-2747rev 1:CAS:528:DC%2BD2MXit1ygsLw%3D
27. J Panyam V Labhasetwar 2003 Biodegradable nanoparticles for drug and gene delivery to cells and tissue Adv Drug Deliv Rev 55 3 329 47 12628320 10.1016/S0169-409X(02)00228-4 1:CAS:528:DC%2BD3sXhs1Cgurw%3D
28. G Tosi L Costantino F Rivasi B Ruozi E Leo AV Vergoni, et al. 2007 Targeting the central nervous system: in vivo experiments with peptide-derivatized nanoparticles loaded with Loperamide and Rhodamine-123 J Control Release 122 1 1 9 17651855 10.1016/j.jconrel.2007.05.022 1:CAS:528:DC%2BD2sXpsV2rtL0%3D
29. L Fenart A Casanova B Dehouck C Duhem S Slupek R Cecchelli, et al. 1999 Evaluation of effect of charge and lipid coating on ability of 60-nm nanoparticles to cross an in vitro model of the blood-brain barrier J Pharmacol Exp Ther 291 3 1017 22 10565819 1:CAS:528:DyaK1MXnslygtLY%3D
30. Y Jallouli A Paillard J Chang E Sevin D Betbeder 2007 Influence of surface charge and inner composition of porous nanoparticles to cross blood-brain barrier in vitro Int J Pharm 344 1-2 103 9 17651930 10.1016/j.ijpharm.2007.06.023 1:CAS:528:DC%2BD2sXhtV2qtLnP
31. P Blasi S Giovagnoli A Schoubben M Ricci C Rossi 2007 Solid lipid nanoparticles for targeted brain drug delivery Adv Drug Deliv Rev 59 6 454 77 17570559 10.1016/j.addr.2007.04.011 1:CAS:528:DC%2BD2sXpt1Cqtrg%3D
32. HR Kim K Andrieux S Gil M Taverna H Chacun D Desmaele, et al. 2007 Translocation of poly(ethylene glycol-co-hexadecyl)cyanoacrylate nanoparticles into rat brain endothelial cells: role of apolipoproteins in receptor-mediated endocytosis Biomacromolecules 8 3 793 9 17309294 10.1021/bm060711a 1:CAS:528:DC%2BD2sXhvVGqurg%3D
33. J Kreuter P Ramge V Petrov S Hamm SE Gelperina B Engelhardt, et al. 2003 Direct evidence that polysorbate-80-coated poly(butylcyanoacrylate) nanoparticles deliver drugs to the CNS via specific mechanisms requiring prior binding of drug to the nanoparticles Pharm Res 20 3 409 16 12669961 10.1023/A:1022604120952 1:CAS:528:DC%2BD3sXhslGrtr8%3D
34. B Dehouck L Fenart MP Dehouck A Pierce G Torpier R Cecchelli 1997 A new function for the LDL receptor: transcytosis of LDL across the blood-brain barrier J Cell Biol 138 4 877 89 9265653 10.1083/jcb.138.4.877 1:CAS:528:DyaK2sXlsleiurg%3D
35. KR Duffy WM Pardridge 1987 Blood-brain barrier transcytosis of insulin in developing rabbits Brain Res 420 1 32 8 3315116 10.1016/0006-8993(87)90236-8 1:CAS:528:DyaL2sXlvFWnsrk%3D
36. L Descamps MP Dehouck G Torpier R Cecchelli 1996 Receptor-mediated transcytosis of transferrin through blood-brain barrier endothelial cells Am J Physiol 270 4 Pt 2 H1149 58 8967351 1:CAS:528:DyaK28Xis1Klur0%3D
37. ZM Qian H Li H Sun K Ho 2002 Targeted drug delivery via the transferrin receptor-mediated endocytosis pathway Pharmacol Rev 54 4 561 87 12429868 10.1124/pr.54.4.561 1:CAS:528:DC%2BD38Xps1Grs7k%3D
38. Y Li M Ogris E Wagner J Pelisek M Ruffer 2003 Nanoparticles bearing polyethyleneglycol-coupled transferrin as gene carriers: preparation and in vitro evaluation Int J Pharm 259 1-2 93 101 12787639 10.1016/S0378-5173(03) 00211-4 1:CAS:528:DC%2BD3sXktF2rtrc%3D
39. X Pan J Guan JW Yoo AJ Epstein LJ Lee RJ Lee 2008 Cationic lipid-coated magnetic nanoparticles associated with transferrin for gene delivery Int J Pharm 358 1-2 263 70 18384982 10.1016/j.ijpharm.2008.02.020 1:CAS:528: DC%2BD1cXmsFagtbg%3D
40. SK Sahoo V Labhasetwar 2005 Enhanced antiproliferative activity of transferrin-conjugated paclitaxel-loaded nanoparticles is mediated via sustained intracellular drug retention Mol Pharm 2 5 373 83 16196490 10.1021/mp050032z 1:CAS:528:DC%2BD2MXltl2gtLo%3D
41. RA Abela J Qian L Xu TS Lawrence M Zhang 2008 Radiation improves gene delivery by a novel transferrin-lipoplex nanoparticle selectively in cancer cells Cancer Gene Ther 15 8 496 507 18483503 10.1038/cgt.2008.26 1:CAS:528:DC%2BD1cXosFSqu7g%3D
42. X Zhang CG Koh B Yu S Liu L Piao G Marcucci, et al. 2009 Transferrin receptor targeted lipopolyplexes for delivery of antisense oligonucleotide g3139 in a murine k562 xenograft model Pharm Res 26 6 1516 24 19291371 10.1007/s11095-009-9864-8 1:CAS:528:DC%2BD1MXjt1Sqs7w%3D
43. NC Bellocq SH Pun GS Jensen ME Davis 2003 Transferrin-containing, cyclodextrin polymer-based particles for tumor-targeted gene delivery Bioconjug Chem 14 6 1122 32 14624625 10.1021/bc034125f 1:CAS:528:DC%2BD3sXos1Cjur0%3D
44. JL Li L Wang XY Liu ZP Zhang HC Guo WM Liu, et al. 2009 In vitro cancer cell imaging and therapy using transferrin-conjugated gold nanoparticles Cancer Lett 274 2 319 26 18977071 10.1016/j.canlet.2008.09.024 1:CAS:528: DC%2BD1MXns12qtQ%3D%3D
45. A Beduneau P Saulnier F Hindre A Clavreul JC Leroux JP Benoit 2007 Design of targeted lipid nanocapsules by conjugation of whole antibodies and antibody Fab' fragments Biomaterials 28 33 4978 90 17716725 10.1016/j.biomaterials.2007. 05.014 1:CAS:528:DC%2BD2sXhtVSktLrP
46. O Dechy-Cabaret B Martin-Vaca D Bourissou 2004 Controlled ring-opening polymerization of lactide and glycolide Chem Rev 104 12 6147 76 15584698 10.1021/cr040002s 1:CAS:528:DC%2BD2cXotVOlt7Y%3D
47. J Chang Y Jallouli M Kroubi XB Yuan W Feng CS Kang, et al. 2009 Characterization of endocytosis of transferrin-coated PLGA nanoparticles by the blood-brain barrier Int J Pharm 379 2 285 92 19416749 10.1016/j.ijpharm.2009.04. 035 1:CAS:528:DC%2BD1MXhtVKjsr3N
48. A Jain G Chasoo SK Singh AK Saxena SK Jain 2011 Transferrin-appended PEGylated nanoparticles for temozolomide delivery to brain: in vitro characterisation J Microencapsul 28 1 21 8 21171813 10.3109/02652048.2010.522257 1:CAS:528:DC%2BC3cXhsFOqtLnF
49. N Shah K Chaudhari P Dantuluri RS Murthy S Das 2009 Paclitaxel-loaded PLGA nanoparticles surface modified with transferrin and Pluronic((R))P85, an in vitro cell line and in vivo biodistribution studies on rat model J Drug Target 17 7 533 42 19530913 10.1080/10611860903046628 1:CAS:528:DC%2BD1MXptVegt7o%3D
50. CW Gan SS Feng 2010 Transferrin-conjugated nanoparticles of poly(lactide)-D-alpha-tocopheryl polyethylene glycol succinate diblock copolymer for targeted drug delivery across the blood-brain barrier Biomaterials 31 30 7748 57 20673685 10.1016/j.biomaterials.2010.06.053 1:CAS:528:DC%2BC3cXhtVGhs73K
51. F Xu W Lu H Wu L Fan X Gao X Jiang 2009 Brain delivery and systemic effect of cationic albumin conjugated PLGA nanoparticles J Drug Target 17 6 423 34 19527113 10.1080/10611860902963013 1:CAS:528:DC%2BD1MXnt1Sisr4%3D
52. GC Ruben JZ Wang K Iqbal I Grundke-Iqbal 2005 Paired helical filaments (PHFs) are a family of single filament structures with a common helical turn period: negatively stained PHF imaged by TEM and measured before and after sonication, deglycosylation, and dephosphorylation Microsc Res Tech 67 3-4 175 95 16104003 10.1002/jemt.20197 1:CAS:528:DC%2BD2MXhtVGmtL3M
53. S Tsuchiya Y Kobayashi Y Goto H Okumura S Nakae T Konno, et al. 1982 Induction of maturation in cultured human monocytic leukemia cells by a phorbol diester Cancer Res 42 4 1530 6 6949641 1:CAS:528:DyaL38Xks1OmsLw%3D
54. KD McCarthy J de Vellis 1980 Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue J Cell Biol 85 3 890 902 6248568 10.1083/jcb.85.3.890 1:CAS:528:DyaL3cXkvFaltL0%3D
55. L Johannes C Lamaze 2002 Clathrin-dependent or not: is it still the question? Traffic 3 7 443 51 12047552 10.1034/j.1600-0854.2002.30701.x 1:CAS:528:DC%2BD38XltF2ltLg%3D
56. SK Rodal G Skretting O Garred F Vilhardt B van Deurs K Sandvig 1999 Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles Mol Biol Cell 10 4 961 74 10198050 1:CAS:528:DyaK1MXisVGks7o%3D
57. JM Larkin MS Brown JL Goldstein RG Anderson 1983 Depletion of intracellular potassium arrests coated pit formation and receptor-mediated endocytosis in fibroblasts Cell 33 1 273 85 6147196 10.1016/0092-8674(83)90356-2 1:CAS:528:DyaL3sXktlKnsLk%3D
58. NQ Liu AS Lossinsky W Popik X Li C Gujuluva B Kriederman, et al. 2002 Human immunodeficiency virus type 1 enters brain microvascular endothelia by macropinocytosis dependent on lipid rafts and the mitogen-activated protein kinase signaling pathway J Virol 76 13 6689 700 12050382 10.1128/JVI.76.13.6689- 6700.2002 1:CAS:528:DC%2BD38XkvVGgs7Y%3D
59. RA Jain 2000 The manufacturing techniques of various drug loaded biodegradable poly(lactide-co-glycolide) (PLGA) devices Biomaterials 21 23 2475 90 11055295 10.1016/S0142-9612(00)00115-0 1:CAS:528:DC%2BD3cXmslKmtL0%3D
60. AL Klibanov K Maruyama VP Torchilin L Huang 1990 Amphipathic polyethyleneglycols effectively prolong the circulation time of liposomes FEBS Lett 268 1 235 7 2384160 10.1016/0014-5793(90)81016-H 1:CAS:528: DyaK3cXmtFOqtbc%3D
61. J Kreuter 1994 Drug targeting with nanoparticles Eur J Drug Metab Pharmacokinet 19 3 253 6 7867668 10.1007/BF03188928 1:CAS:528:DyaK2MXitlSjt7o%3D
62. A Vonarbourg C Passirani P Saulnier JP Benoit 2006 Parameters influencing the stealthiness of colloidal drug delivery systems Biomaterials 27 24 4356 73 16650890 10.1016/j.biomaterials.2006.03.039 1:CAS:528:DC%2BD28XksFyns7g%3D
63. M Daigneault JA Preston HM Marriott MK Whyte DH Dockrell 2010 The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages PLoS One 5 1 e8668 20084270 10.1371/journal.pone.0008668
64. T Hirata PB Bitterman JF Mornex RG Crystal 1986 Expression of the transferrin receptor gene during the process of mononuclear phagocyte maturation J Immunol 136 4 1339 45 3003194 1:CAS:528:DyaL28Xht1yju78%3D
65. S Matveev DR van der Westhuyzen EJ Smart 1999 Co-expression of scavenger receptor-BI and caveolin-1 is associated with enhanced selective cholesteryl ester uptake in THP-1 macrophages J Lipid Res 40 9 1647 54 10484611 1:CAS:528:DyaK1MXmtVajt7s%3D
66. AP Liu F Aguet G Danuser SL Schmid 2010 Local clustering of transferrin receptors promotes clathrin-coated pit initiation J Cell Biol 191 7 1381 93 21187331 10.1083/jcb.201008117 1:CAS:528:DC%2BC3MXis1Wjug%3D%3D
67. RJ Davis S Corvera MP Czech 1986 Insulin stimulates cellular iron uptake and causes the redistribution of intracellular transferrin receptors to the plasma membrane J Biol Chem 261 19 8708 11 3013860 1:CAS:528:DyaL28XksFCqtL4%3D
68. T Galvez MN Teruel WD Heo JT Jones ML Kim J Liou, et al. 2007 siRNA screen of the human signaling proteome identifies the PtdIns(3,4,5)P3-mTOR signaling pathway as a primary regulator of transferrin uptake Genome Biol 8 7 R142 17640392 10.1186/gb-2007-8-7-r142
69. SW Schneider T Ludwig L Tatenhorst S Braune H Oberleithner V Senner, et al. 2004 Glioblastoma cells release factors that disrupt blood-brain barrier features Acta Neuropathol 107 3 272 6 14730455 10.1007/s00401-003-0810-2
70. DB Kirpotin DC Drummond Y Shao MR Shalaby K Hong UB Nielsen, et al. 2006 Antibody targeting of long-circulating lipidic nanoparticles does not increase tumor localization but does increase internalization in animal models Cancer Res 66 13 6732 40 16818648 10.1158/0008-5472.CAN-05-4199 1:CAS:528: DC%2BD28XmsVamu7Y%3D
71. S Acharya SK Sahoo 2011 PLGA nanoparticles containing various anticancer agents and tumour delivery by EPR effect Adv Drug Deliv Rev 63 3 170 83 20965219 10.1016/j.addr.2010.10.008 1:CAS:528:DC%2BC3MXktF2juro%3D